{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T20:41:33Z","timestamp":1790455293921,"version":"4.1.0"},"reference-count":93,"publisher":"MDPI AG","issue":"10","license":[{"start":{"date-parts":[[2020,5,19]],"date-time":"2020-05-19T00:00:00Z","timestamp":1589846400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007917","name":"Agricultural Research Service","doi-asserted-by":"publisher","award":["Project 5030-21220-006-00D"],"award-info":[{"award-number":["Project 5030-21220-006-00D"]}],"id":[{"id":"10.13039\/100007917","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Iron deficiency chlorosis (IDC) is a global crop production problem, significantly impacting yield. However, most IDC studies have focused on model species, not agronomically important crops. Soybean is the second largest crop grown in the United States, yet the calcareous soils across most of the upper U.S. Midwest limit soybean growth and profitability. To understand early soybean iron stress responses, we conducted whole genome expression analyses (RNA-sequencing) of leaf and root tissue from the iron efficient soybean (Glycine max) cultivar Clark, at 30, 60 and 120 min after transfer to iron stress conditions. We identified over 10,000 differentially expressed genes (DEGs), with the number of DEGs increasing over time in leaves, but decreasing over time in roots. To investigate these responses, we clustered our expression data across time to identify suites of genes, their biological functions, and the transcription factors (TFs) that regulate their expression. These analyses reveal the hallmarks of the soybean iron stress response (iron uptake and homeostasis, defense, and DNA replication and methylation) can be detected within 30 min. Furthermore, they suggest root to shoot signaling initiates early iron stress responses representing a novel paradigm for crop stress adaptations.<\/jats:p>","DOI":"10.3390\/ijms21103591","type":"journal-article","created":{"date-parts":[[2020,5,20]],"date-time":"2020-05-20T02:48:24Z","timestamp":1589942904000},"page":"3591","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Examining Short-Term Responses to a Long-Term Problem: RNA-Seq Analyses of Iron Deficiency Chlorosis Tolerant Soybean"],"prefix":"10.3390","volume":"21","author":[{"given":"Adrienne N. Moran","family":"Lauter","sequence":"first","affiliation":[{"name":"Corn Insects and Crop Genetics Research Unit, USDA-Agricultural Research Service, Ames, IA 50011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2123-3949","authenticated-orcid":false,"given":"Lindsay","family":"Rutter","sequence":"additional","affiliation":[{"name":"Department of Statistics, Iowa State University, Ames, IA 50011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dianne","family":"Cook","sequence":"additional","affiliation":[{"name":"Department of Econometrics and Business Statistics, Monash University, Clayton VIC 3800, Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jamie A.","family":"O\u2019Rourke","sequence":"additional","affiliation":[{"name":"Corn Insects and Crop Genetics Research Unit, USDA-Agricultural Research Service, Ames, IA 50011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle A.","family":"Graham","sequence":"additional","affiliation":[{"name":"Corn Insects and Crop Genetics Research Unit, USDA-Agricultural Research Service, Ames, IA 50011, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,5,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1016\/S0005-2728(99)00043-2","article-title":"The biogenesis and assembly of photosynthetic proteins in thylakoid membranes","volume":"1411","author":"Wollman","year":"1999","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1105\/tpc.011817","article-title":"PAA1, a P-type ATPase of Arabidopsis, functions in copper transport in chloroplasts","volume":"15","author":"Shikanai","year":"2003","journal-title":"Plant Cell"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1080\/00380768.2004.10408564","article-title":"Iron deficiency of soybean in the north central US and associated soil properties","volume":"50","author":"Hansen","year":"2004","journal-title":"Soil Sci. Plant Nutr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1081\/PLN-100106980","article-title":"Seed treatment, seeding rate and cultivar effects on iron deficiency chlorosis of soybean","volume":"24","author":"Goos","year":"2001","journal-title":"J. Plant Nutr."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"796","DOI":"10.1104\/pp.102.016089","article-title":"Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals","volume":"132","author":"Vert","year":"2003","journal-title":"Plant Physiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"396","DOI":"10.4161\/psb.3.6.5419","article-title":"Long-distance signaling of iron deficiency in plants","volume":"3","author":"Enomoto","year":"2008","journal-title":"Plant Signal. Behav."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1105\/tpc.111.092973","article-title":"Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution","volume":"24","author":"Giehl","year":"2012","journal-title":"Plant Cell"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1455","DOI":"10.1093\/mp\/ssu067","article-title":"OPT3 is a component of the iron-signaling network between leaves and roots and misregulation of OPT3 leads to an over-accumulation of cadmium in seeds","volume":"7","author":"Xie","year":"2014","journal-title":"Mol. Plant"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"2249","DOI":"10.1105\/tpc.114.123737","article-title":"OPT3 is a phloem-specific iron transporter that is essential for systemic iron signaling and redistribution of iron and cadmium in Arabidopsis","volume":"26","author":"Zhai","year":"2014","journal-title":"Plant Cell"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1739","DOI":"10.1093\/pcp\/pcy145","article-title":"The putative peptide gene FEP1 regulates iron deficiency response in Arabidopsis","volume":"59","author":"Hirayama","year":"2018","journal-title":"Plant Cell Physiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3400","DOI":"10.1105\/tpc.104.024315","article-title":"The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response","volume":"16","author":"Colangelo","year":"2004","journal-title":"Plant Cell"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1038\/17800","article-title":"A ferric-chelate reductase for iron uptake from soils","volume":"397","author":"Robinson","year":"1999","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1105\/tpc.001388","article-title":"IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth","volume":"14","author":"Vert","year":"2002","journal-title":"Plant Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1104\/pp.113.228544","article-title":"Feruloyl-CoA 6\u2032-Hydroxylase1-dependent coumarins mediate iron acquisition from alkaline substrates in Arabidopsis","volume":"164","author":"Schmid","year":"2014","journal-title":"Plant Physiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"276","DOI":"10.1016\/j.pbi.2007.04.003","article-title":"Iron utilization and metabolism in plants","volume":"10","author":"Briat","year":"2007","journal-title":"Curr. Opin. Plant Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/j.bbamcr.2006.05.014","article-title":"Molecular aspects of Cu, Fe and Zn homeostasis in plants","volume":"1763","author":"Grotz","year":"2006","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"522","DOI":"10.1111\/j.1399-3054.1993.tb01367.x","article-title":"Nicotianamine: Mediator of transport of iron and heavy metals in the phloem?","volume":"88","author":"Stephan","year":"1993","journal-title":"Physiol. Plant"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1016\/j.plaphy.2011.01.019","article-title":"A new model involving ethylene, nitric oxide and Fe to explain the regulation of Fe-acquisition genes in Strategy I plants","volume":"49","author":"Romera","year":"2011","journal-title":"Plant Physiol. Biochem."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e1179418","DOI":"10.1080\/15592324.2016.1179418","article-title":"Roles of chemical signals in regulation of the adaptive responses to iron deficiency","volume":"11","author":"Liu","year":"2016","journal-title":"Plant Signal. Behav."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.devcel.2016.03.022","article-title":"Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses","volume":"37","author":"Wild","year":"2016","journal-title":"Dev. Cell"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4179","DOI":"10.1093\/jxb\/erw196","article-title":"Involvement of endogenous salicylic acid in iron-deficiency responses in Arabidopsis","volume":"67","author":"Shen","year":"2016","journal-title":"J. Exp. Bot."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"716","DOI":"10.3389\/fpls.2015.00716","article-title":"Local and systemic signaling of iron status and its interactions with homeostasis of other essential elements","volume":"6","author":"Gayomba","year":"2015","journal-title":"Front. Plant Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1111\/pce.12147","article-title":"Replication protein A subunit 3 and the iron efficiency response in soybean","volume":"37","author":"Atwood","year":"2014","journal-title":"Plant Cell Environ."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Buckhout, T.J., Yang, T.J., and Schmidt, W. (2009). Early iron-deficiency-induced transcriptional changes in Arabidopsis roots as revealed by microarray analyses. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-147"},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Moran Lauter, A.N., Peiffer, G.A., Yin, T., Whitham, S.A., Cook, D., Shoemaker, R.C., and Graham, M.A. (2014). Identification of candidate genes involved in early iron deficiency chlorosis signaling in soybean (Glycine max) roots and leaves. BMC Genom., 15.","DOI":"10.1186\/1471-2164-15-702"},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"O\u2019Rourke, J.A., Charlson, D.V., Gonzalez, D.O., Vodkin, L.O., Graham, M.A., Cianzio, S.R., Grusak, M.A., and Shoemaker, R.C. (2007). Microarray analysis of iron deficiency chlorosis in near-isogenic soybean lines. BMC Genom., 8.","DOI":"10.1186\/1471-2164-8-476"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"O\u2019Rourke, J.A., Nelson, R.T., Grant, D., Schmutz, J., Grimwood, J., Cannon, S., Vance, C.P., Graham, M.A., and Shoemaker, R.C. (2009). Integrating microarray analysis and the soybean genome to understand the soybeans iron deficiency response. BMC Genom., 10.","DOI":"10.1186\/1471-2164-10-376"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1745","DOI":"10.1104\/pp.111.189860","article-title":"Identification of candidate genes underlying an iron efficiency quantitative trait locus in soybean","volume":"158","author":"Peiffer","year":"2012","journal-title":"Plant Physiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1093\/jxb\/err343","article-title":"Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots","volume":"63","author":"Stein","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1111\/nph.12911","article-title":"Transcriptomic and physiological characterization of the fefe mutant of melon (Cucumis melo) reveals new aspects of iron-copper crosstalk","volume":"203","author":"Waters","year":"2014","journal-title":"New Phytol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"5903","DOI":"10.1093\/jxb\/ers239","article-title":"Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana","volume":"63","author":"Waters","year":"2012","journal-title":"J. Exp. Bot."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1038\/nature08670","article-title":"Genome sequence of the palaeopolyploid soybean","volume":"463","author":"Schmutz","year":"2010","journal-title":"Nature"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"edgeR: A Bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"ref_34","unstructured":"Fisher, R.A. (1966). The Design of Experiments, London Oliver & Boyd. [8th ed.]."},{"key":"ref_35","unstructured":"Bonferroni, C.E. (1935). Ill Calcolo delle assicurazioni su gruppi di teste. Studi in Onore del Professore Salvatore Ortu Carboni, Bardi."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1104\/pp.104.040071","article-title":"Functional annotation of the Arabidopsis genome using controlled vocabularies","volume":"135","author":"Berardini","year":"2004","journal-title":"Plant Physiol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Wang, Z., Libault, M., Joshi, T., Valliyodan, B., Nguyen, H.T., Xu, D., Stacey, G., and Cheng, J. (2010). SoyDB: A knowledge database of soybean transcription factors. BMC Plant Biol., 10.","DOI":"10.1186\/1471-2229-10-14"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"2263","DOI":"10.1111\/pce.13192","article-title":"Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots","volume":"41","author":"Khan","year":"2018","journal-title":"Plant Cell Environ."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.1104\/pp.113.220426","article-title":"Mutually exclusive alterations in secondary metabolism are critical for the uptake of insoluble iron compounds by Arabidopsis and Medicago truncatula","volume":"162","author":"Lin","year":"2013","journal-title":"Plant Physiol."},{"key":"ref_40","first-page":"254","article-title":"Iron deficiency in plants: An insight from proteomic approaches","volume":"4","author":"Grusak","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_41","first-page":"321","article-title":"Dynamic gene expression changes in response to micronutrient, macronutrient, and multiple stress exposures in soybean","volume":"20","author":"McCabe","year":"2019","journal-title":"Funct. Integr. Genom."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"D447","DOI":"10.1093\/nar\/gku1003","article-title":"STRING v10: Protein\u2013protein interaction networks, integrated over the tree of life","volume":"43","author":"Szklarczyk","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1080\/19491034.2016.1276142","article-title":"MGO3 and GIP1 act synergistically for the maintenance of centromeric cohesion","volume":"8","author":"Batzenschlager","year":"2017","journal-title":"Nucleus"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1111\/pce.13365","article-title":"BRUSHY1\/TONSOKU\/MGOUN3 is required for heat stress memory","volume":"42","author":"Brzezinka","year":"2018","journal-title":"Plant Cell Environ."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1146\/annurev-phyto-080614-120132","article-title":"Priming for enhanced defense","volume":"53","author":"Conrath","year":"2015","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.1007\/s00018-014-1792-z","article-title":"Stress-induced chromatin changes in plants: Of memories, metabolites and crop improvement","volume":"72","author":"Vriet","year":"2015","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e30674","DOI":"10.7554\/eLife.30674","article-title":"DDM1 and Lsh remodelers allow methylation of DNA wrapped in nucleosomes","volume":"6","author":"Lyons","year":"2017","journal-title":"Elife"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1470","DOI":"10.1093\/mp\/ssu079","article-title":"Arabidopsis VIM proteins regulate epigenetic silencing by modulating DNA methylation and histone modification in cooperation with MET1","volume":"7","author":"Kim","year":"2014","journal-title":"Mol. Plant"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1111\/tpj.13499","article-title":"RAD 54 forms DNA repair foci in response to DNA damage in living plant cells","volume":"90","author":"Hirakawa","year":"2017","journal-title":"Plant J."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"e46085","DOI":"10.15252\/embr.201846085","article-title":"Dual localized kinesin-12 POK2 plays multiple roles during cell division and interacts with MAP65-3","volume":"19","author":"Herrmann","year":"2018","journal-title":"EMBO Rep."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"6537","DOI":"10.1016\/j.febslet.2006.11.002","article-title":"Gain-and loss-of-function mutations in Zat10 enhance the tolerance of plants to abiotic stress","volume":"580","author":"Mittler","year":"2006","journal-title":"FEBS Lett."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2015","DOI":"10.1007\/s00299-014-1675-7","article-title":"ZAT11, a zinc finger transcription factor, is a negative regulator of nickel ion tolerance in Arabidopsis","volume":"33","author":"Liu","year":"2014","journal-title":"Plant Cell Rep."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1648","DOI":"10.1104\/pp.109.138990","article-title":"The role of WRKY transcription factors in plant immunity","volume":"150","author":"Pandey","year":"2009","journal-title":"Plant Physiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.3389\/fpls.2017.01015","article-title":"Extra large G-protein interactome reveals multiple stress response function and partner-dependent XLG subcellular localization","volume":"8","author":"Liang","year":"2017","journal-title":"Front. Plant Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"493","DOI":"10.1016\/j.molcel.2017.12.026","article-title":"A regulatory module controlling homeostasis of a plant immune kinase","volume":"69","author":"Wang","year":"2018","journal-title":"Mol. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1104\/pp.110.1.329","article-title":"Shoot-to-root signal transmission regulates root Fe (III) reductase activity in the dgl mutant of pea","volume":"110","author":"Grusak","year":"1996","journal-title":"Plant Physiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1679","DOI":"10.1104\/pp.125.4.1679","article-title":"Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability","volume":"125","author":"Schikora","year":"2001","journal-title":"Plant Physiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1007\/s00425-007-0596-x","article-title":"Long-distance signals positively regulate the expression of iron uptake genes in tobacco roots","volume":"227","author":"Enomoto","year":"2007","journal-title":"Planta"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Garnica, M., Bacaicoa, E., Mora, V., San Francisco, S., Baigorri, R., Zamarre\u00f1o, A.M., and Garcia-Mina, J.M. (2018). Shoot iron status and auxin are involved in iron deficiency-induced phytosiderophores release in wheat. BMC Plant Biol., 18.","DOI":"10.1186\/s12870-018-1324-3"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"757","DOI":"10.3389\/fpls.2018.00757","article-title":"Shoot-root communication plays a key role in physiological alterations of rice (Oryza sativa) under iron deficiency","volume":"9","author":"Chen","year":"2018","journal-title":"Front. Plant Sci."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"254","DOI":"10.2135\/cropsci1998.0011183X003800010043x","article-title":"Field and nutrient solution tests measure similar mechanisms controlling iron deficiency chlorosis in soybean","volume":"38","author":"Lin","year":"1998","journal-title":"Crop. Sci."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1915","DOI":"10.1080\/01904160009382153","article-title":"Nutrient solution screening of Fe chlorosis resistance in soybean evaluated by molecular characterization","volume":"23","author":"Lin","year":"2000","journal-title":"J. Plant Nutr."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1929","DOI":"10.1080\/01904160009382154","article-title":"Molecular characterization of iron deficiency chlorosis in soybean","volume":"23","author":"Lin","year":"2000","journal-title":"J. Plant Nutr."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1104\/pp.110.158949","article-title":"An integrative approach to genomic introgression mapping","volume":"154","author":"Severin","year":"2010","journal-title":"Plant Physiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"104","DOI":"10.3389\/fpls.2013.00104","article-title":"Genomic heterogeneity and structural variation in soybean near isogenic lines","volume":"4","author":"Stec","year":"2013","journal-title":"Front. Plant Sci."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Assefa, T., Zhang, J., Chowda-Reddy, R., Lauter, A.N.M., Singh, A., O\u2019Rourke, J.A., Graham, M.A., and Singh, A.K. (2020). Deconstructing the genetic architecture of iron deficiency chlorosis in soybean using genome-wide approaches. BMC Plant Biol., 20.","DOI":"10.1186\/s12870-020-2237-5"},{"key":"ref_67","unstructured":"Boerma, H.R., and Specht, J.E. (2004). Speciation and cytogenetics. Soybeans: Improvement, Production and Uses, American Society of Agronomy, Crop Science Society of America, Soil Science Society of America. [3rd ed.]."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.2135\/cropsci2013.10.0665","article-title":"Genetic improvement of U.S. Soybean in maturity groups II, III and IV","volume":"54","author":"Rincker","year":"2014","journal-title":"Crop. Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"690","DOI":"10.2134\/agronj1958.00021962005000110016x","article-title":"Registration of soybean varities, VI","volume":"50","author":"Johnson","year":"1958","journal-title":"Agron. J."},{"key":"ref_70","unstructured":"(2020, May 19). Germplasm Resources Information Network (GRIN) National Genetic Resources Program, Available online: https:\/\/www.ars-grin.gov."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"2063","DOI":"10.1080\/01904169209364459","article-title":"Detailed method to screen dicot cultivars for resistance to Fe-chlorosis using FeDTPA and bicarbonate in nutrient solutions","volume":"15","author":"Chaney","year":"1992","journal-title":"J. Plant Nutr."},{"key":"ref_72","unstructured":"Buffalo, V. (2020, May 19). Scythe-a Bayesian Adaptor Trimmer. Available online: https:\/\/github.com\/vsbuffalo\/scythe."},{"key":"ref_73","unstructured":"(2020, May 19). The FASTX-Toolkit. FASTQ\/A Short-Reads Pre-Processing Tools. Available online: http:\/\/hannonlab.cshl.edu\/fastx_toolkit\/."},{"key":"ref_74","unstructured":"(2020, May 19). Sickle-A Windowed Adaptive Trimming Tool for FASTQ Files Using Quality. Available online: https:\/\/github.com\/najoshi\/sickle."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1093\/bioinformatics\/btp120","article-title":"TopHat: Discovering splice junctions with RNA-Seq","volume":"25","author":"Trapnell","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"1000 Genome Project Data Processing Subgroup, The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_77","unstructured":"R Core Team (2018). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."},{"key":"ref_78","unstructured":"Morgan, M., and Pages, H. (2013). Rsamtools: Binary Alignment (BAM), Variant Call (BCF), or Tabix File Import (R Package Version 1.12.4), R Foundation for Statistical Computing."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1093\/bioinformatics\/btp328","article-title":"rtracklayer: An R package for interfacing with genome browsers","volume":"25","author":"Lawrence","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_80","doi-asserted-by":"crossref","unstructured":"Lawrence, M., Huber, W., Pages, H., Aboyoun, P., Carlson, M., Gentleman, R., Morgan, M.T., and Carey, V.J. (2013). Software for computing and annotating genomic ranges. PLoS Comput. Biol., 9.","DOI":"10.1371\/journal.pcbi.1003118"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"4288","DOI":"10.1093\/nar\/gks042","article-title":"Differential expression analysis of multifactor RNA-Seq experiments with respect to biological variation","volume":"40","author":"McCarthy","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"2881","DOI":"10.1093\/bioinformatics\/btm453","article-title":"Moderated statistical tests for assessing differences in tag abundance","volume":"23","author":"Robinson","year":"2007","journal-title":"Bioinformatics"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"e91","DOI":"10.1093\/nar\/gku310","article-title":"Robustly detecting differential expression in RNA sequencing data using observation weights","volume":"42","author":"Zhou","year":"2014","journal-title":"Nucleic Acids Res."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"R25","DOI":"10.1186\/gb-2010-11-3-r25","article-title":"A scaling normalization method for differential expression analysis of RNA-seq data","volume":"11","author":"Robinson","year":"2010","journal-title":"Genome Biol."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Wickham, H. (2009). Ggplot2: Elegant graphics for data analysis. Use R!, Springer.","DOI":"10.1007\/978-0-387-98141-3"},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Rutter, L., Moran Lauter, A.N., Graham, M.A., and Cook, D. (2019). Visualization methods for differential expression analysis. BMC Bioinform., 20.","DOI":"10.1186\/s12859-019-2968-1"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"321","DOI":"10.1093\/biostatistics\/kxm030","article-title":"Small-sample estimation of negative binomial dispersion, with applications to SAGE data","volume":"9","author":"Robinson","year":"2007","journal-title":"Biostatistics"},{"key":"ref_88","unstructured":"(2020, May 19). The SoyBase Genome Annotation Report Page. Available online: http:\/\/soybase.org\/genomeannotation.index.php."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/nar\/25.17.3389","article-title":"Gapped BLAST and PSI-BLAST: A new generation of protein database search programs","volume":"25","author":"Altschul","year":"1997","journal-title":"Nucleic Acids Res."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"82","DOI":"10.1093\/comjnl\/28.1.82","article-title":"A survey of algorithms for contiguity-constrained clustering and related problems","volume":"28","author":"Murtagh","year":"1985","journal-title":"Comput. J."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"274","DOI":"10.1007\/s00357-014-9161-z","article-title":"Ward\u2019s hierarchical agglomerative clustering method: Which algorithms implement ward\u2019s criterion?","volume":"31","author":"Murtagh","year":"2014","journal-title":"J. Class."},{"key":"ref_92","unstructured":"(2020, May 19). The SoyBase GO Term Enrichment Tool. Available online: https:\/\/www.soybase.org\/goslimgraphic_v2\/dashboard.php."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"1029","DOI":"10.1071\/FP12296","article-title":"Transcriptome analyses and virus induced gene silencing identify genes in the Rpp4-mediated Asian soybean rust resistance pathway","volume":"40","author":"Morales","year":"2013","journal-title":"Funct. Plant Biol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/10\/3591\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:30:26Z","timestamp":1760175026000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/10\/3591"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,19]]},"references-count":93,"journal-issue":{"issue":"10","published-online":{"date-parts":[[2020,5]]}},"alternative-id":["ijms21103591"],"URL":"https:\/\/doi.org\/10.3390\/ijms21103591","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,19]]}}}